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The tectonic complex regulates membrane protein composition in the photoreceptor cilium

The primary cilium is a signaling organelle with a unique membrane composition maintained by a diffusional barrier residing at the transition zone. Many transition zone proteins, such as the tectonic complex, are linked to preserving ciliary composition but the mechanism remains unknown. To understa...

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Autores principales: Truong, Hanh M., Cruz-Colón, Kevin O., Martínez-Márquez, Jorge Y., Willer, Jason R., Travis, Amanda M., Biswas, Sondip K., Lo, Woo-Kuen, Bolz, Hanno J., Pearring, Jillian N.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
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Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10500017/
https://www.ncbi.nlm.nih.gov/pubmed/37704658
http://dx.doi.org/10.1038/s41467-023-41450-z
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author Truong, Hanh M.
Cruz-Colón, Kevin O.
Martínez-Márquez, Jorge Y.
Willer, Jason R.
Travis, Amanda M.
Biswas, Sondip K.
Lo, Woo-Kuen
Bolz, Hanno J.
Pearring, Jillian N.
author_facet Truong, Hanh M.
Cruz-Colón, Kevin O.
Martínez-Márquez, Jorge Y.
Willer, Jason R.
Travis, Amanda M.
Biswas, Sondip K.
Lo, Woo-Kuen
Bolz, Hanno J.
Pearring, Jillian N.
author_sort Truong, Hanh M.
collection PubMed
description The primary cilium is a signaling organelle with a unique membrane composition maintained by a diffusional barrier residing at the transition zone. Many transition zone proteins, such as the tectonic complex, are linked to preserving ciliary composition but the mechanism remains unknown. To understand tectonic’s role, we generate a photoreceptor-specific Tctn1 knockout mouse. Loss of Tctn1 results in the absence of the entire tectonic complex and associated MKS proteins yet has minimal effects on the transition zone structure of rod photoreceptors. We find that the protein composition of the photoreceptor cilium is disrupted as non-resident membrane proteins accumulate in the cilium over time, ultimately resulting in photoreceptor degeneration. We further show that fluorescent rhodopsin moves faster through the transition zone in photoreceptors lacking tectonic, which suggests that the tectonic complex acts as a physical barrier to slow down membrane protein diffusion in the photoreceptor transition zone to ensure proper removal of non-resident membrane proteins.
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spelling pubmed-105000172023-09-15 The tectonic complex regulates membrane protein composition in the photoreceptor cilium Truong, Hanh M. Cruz-Colón, Kevin O. Martínez-Márquez, Jorge Y. Willer, Jason R. Travis, Amanda M. Biswas, Sondip K. Lo, Woo-Kuen Bolz, Hanno J. Pearring, Jillian N. Nat Commun Article The primary cilium is a signaling organelle with a unique membrane composition maintained by a diffusional barrier residing at the transition zone. Many transition zone proteins, such as the tectonic complex, are linked to preserving ciliary composition but the mechanism remains unknown. To understand tectonic’s role, we generate a photoreceptor-specific Tctn1 knockout mouse. Loss of Tctn1 results in the absence of the entire tectonic complex and associated MKS proteins yet has minimal effects on the transition zone structure of rod photoreceptors. We find that the protein composition of the photoreceptor cilium is disrupted as non-resident membrane proteins accumulate in the cilium over time, ultimately resulting in photoreceptor degeneration. We further show that fluorescent rhodopsin moves faster through the transition zone in photoreceptors lacking tectonic, which suggests that the tectonic complex acts as a physical barrier to slow down membrane protein diffusion in the photoreceptor transition zone to ensure proper removal of non-resident membrane proteins. Nature Publishing Group UK 2023-09-13 /pmc/articles/PMC10500017/ /pubmed/37704658 http://dx.doi.org/10.1038/s41467-023-41450-z Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Truong, Hanh M.
Cruz-Colón, Kevin O.
Martínez-Márquez, Jorge Y.
Willer, Jason R.
Travis, Amanda M.
Biswas, Sondip K.
Lo, Woo-Kuen
Bolz, Hanno J.
Pearring, Jillian N.
The tectonic complex regulates membrane protein composition in the photoreceptor cilium
title The tectonic complex regulates membrane protein composition in the photoreceptor cilium
title_full The tectonic complex regulates membrane protein composition in the photoreceptor cilium
title_fullStr The tectonic complex regulates membrane protein composition in the photoreceptor cilium
title_full_unstemmed The tectonic complex regulates membrane protein composition in the photoreceptor cilium
title_short The tectonic complex regulates membrane protein composition in the photoreceptor cilium
title_sort tectonic complex regulates membrane protein composition in the photoreceptor cilium
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10500017/
https://www.ncbi.nlm.nih.gov/pubmed/37704658
http://dx.doi.org/10.1038/s41467-023-41450-z
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